Skip to main content

Advertisement

SpringerLink
Log in

A Broad Application of CRISPR Cas9 in Infectious Diseases of Central Nervous System

  • Invited Review
  • Published:
Journal of Neuroimmune Pharmacology Aims and scope Submit manuscript

Abstract

Virus-induced diseases or neurological complications are huge socio-economic burden to human health globally. The complexity of viral-mediated CNS pathology is exacerbated by reemergence of new pathogenic neurotropic viruses of high public relevance. Although the central nervous system is considered as an immune privileged organ and is mainly protected by barrier system, there are a vast majority of neurotropic viruses capable of gaining access and cause diseases. Despite continued growth of the patient population and a number of treatment strategies, there is no successful viral specific therapy available for viral induced CNS diseases. Therefore, there is an urgent need for a clear alternative treatment strategy that can effectively target neurotropic viruses of DNA or RNA genome. To address this need, rapidly growing gene editing technology based on CRISPR/Cas9, provides unprecedented control over viral genome editing and will be an effective, highly specific and versatile tool for targeting CNS viral infection. In this review, we discuss the application of this system to control CNS viral infection and associated neurological disorders and future prospects.

CRISPR/Cas9 technology as agent control over CNS viral infection.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abudayyeh OO, Gootenberg JS, Konermann S, Joung J, Slaymaker IM, Cox DB, Shmakov S, Makarova KS, Semenova E, Minakhin L, Severinov K, Regev A, Lander ES, Koonin EV, Zhang F (2016) C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science 353:aaf5573. https://doi.org/10.1126/science.aaf5573

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ali Z, Ali S, Tashkandi M, Zaidi SS, Mahfouz MM (2016) CRISPR/Cas9-mediated immunity to geminiviruses: differential interference and evasion. Sci Rep 6:26912. https://doi.org/10.1038/srep26912

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Alimonti JB, Ball TB, Fowke KR (2003) Mechanisms of CD4+ T lymphocyte cell death in human immunodeficiency virus infection and AIDS. J Gen Virol 84:1649–1661

    PubMed  CAS  Google Scholar 

  • Archin NM, Liberty AL, Kashuba AD, Choudhary SK, Kuruc JD, Crooks AM. ... Richman DD (2012) Administration of vorinostat disrupts HIV-1 latency in patients on antiretroviral therapy. Nature 487(7408): 482

    PubMed  PubMed Central  CAS  Google Scholar 

  • Arduino PG, Porter SR (2008) Herpes simplex virus type 1 infection: overview on relevant clinico-pathological features. J Oral Pathol Med 37:107–121

    PubMed  Google Scholar 

  • Arzumanyan A, Reis HM, Feitelson MA (2013) Pathogenic mechanisms in HBV-and HCV-associated hepatocellular carcinoma. Nat Rev Cancer 13:123–135

    PubMed  CAS  Google Scholar 

  • Azevedo LS, Pierrotti LC, Abdala E, Costa SF, Strabelli TM, Campos SV, Ramos JF, Latif AZ, Litvinov N, Maluf NZ, Caiaffa Filho HH, Pannuti CS, Lopes MH, Santos VA, Linardi Cda C, Yasuda MA, Marques HH (2015) Cytomegalovirus infection in transplant recipients. Clinics (Sao Paulo) 70:515–523

    Google Scholar 

  • Badia R, Ballana E, Castellví M, García-Vidal E, Pujantell M, Clotet B, Prado JG, Puig J, Martínez MA, Riveira-Muñoz E, Esté JA (2018) CD32 expression is associated to T-cell activation and is not a marker of the HIV-1 reservoir. Nat Commun 9:2739. https://doi.org/10.1038/s41467-018-05157-w

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bak RO, Gomez-Ospina N, Porteus MH (2018) Gene editing on center stage. Trends Genet 34:600–611

    PubMed  CAS  Google Scholar 

  • Barrangou R, Doudna JA (2016) Applications of CRISPR technologies in research and beyond. Nat Biotechnol 34:933–941

    PubMed  CAS  Google Scholar 

  • Bayat H, Naderi F, Khan AH, Memarnejadian A, Rahimpour A (2018) The impact of CRISPR-Cas system on antiviral therapy. Adv Pharm Bull 8:591–597

    PubMed  PubMed Central  CAS  Google Scholar 

  • Bearer EL (2012) HSV, axonal transport and Alzheimer’s disease: in vitro and in vivo evidence for causal relationships. Futur Virol 7(9):885–899

    CAS  Google Scholar 

  • Bella R, Kaminski R, Mancuso P, Young WB, Chen C, Sariyer R ... Kashanchi F (2018) Removal of HIV DNA by CRISPR from patient blood engrafts in humanized mice. Mol Ther-Nucleic Acids 12: 275–282

    PubMed  PubMed Central  CAS  Google Scholar 

  • Bialek JK, Dunay GA, Voges M, Schäfer C, Spohn M, Stucka R et al (2016) Targeted HIV-1 latency reversal using CRISPR/Cas9-derived transcriptional activator systems. PLoS One 11(6):e0158294

    PubMed  PubMed Central  Google Scholar 

  • Biron KK, Fyfe JA, Stanat SC, Leslie LK, Sorrell JB, Lambe CU, Coen DM (1986) A human cytomegalovirus mutant resistant to the nucleoside analog 9-([2-hydroxy-1-(hydroxymethyl) ethoxy] methyl) guanine (BW B759U) induces reduced levels of BW B759U triphosphate. Proc Natl Acad Sci U S A 83:8769–8773

    PubMed  PubMed Central  CAS  Google Scholar 

  • Block TM, Gish R, Guo H, Mehta A, Cuconati A, London WT, Guo JT (2013) Chronic hepatitis B: what should be the goal for new therapies? Antivir Res 98(1):27–34

    PubMed  CAS  Google Scholar 

  • Bloom K, Maepa MB, Ely A, Arbuthnot P: Gene therapy for chronic HBV- can we eliminate cccDNA? Genes (Basel) 9:piiE207. https://doi.org/10.3390/genes9040207

    PubMed Central  Google Scholar 

  • Bogerd HP, Kornepati AV, Marshall JB, Kennedy EM, Cullen BR (2015) Specific induction of endogenous viral restriction factors using CRISPR/Cas-derived transcriptional activators. Proc Natl Acad Sci 112(52):E7249–E7256

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bollen Y, Post J, Koo BK, Snippert HJ (2018) How to create state-of-the-art genetic model systems: strategies for optimal CRISPR-mediated genome editing. Nucleic Acids Res 46(13):6435–6454

    PubMed  PubMed Central  CAS  Google Scholar 

  • Bolotin A, Quinquis B, Sorokin A, Ehrlich SD (2005) Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 151:2551–2561

    PubMed  CAS  Google Scholar 

  • Carroll KJ, Makarewich CA, McAnally J, Anderson DM, Zentilin L, Liu N, Giacca M, Bassel-Duby R, Olson EN (2016) A mouse model for adult cardiac-specific gene deletion with CRISPR/Cas9. Proc Natl Acad Sci U S A 113:338–343

    PubMed  CAS  Google Scholar 

  • Casini A, Olivieri M, Petris G, Montagna C, Reginato G, Maule G, Lorenzin F, Prandi D, Romanel A, Demichelis F, Inga A, Cereseto A (2018) A highly specific SpCas9 variant is identified by in vivo screening in yeast. Nat Biotechnol 36:265–271

    PubMed  PubMed Central  CAS  Google Scholar 

  • Chang J, Guo JT (2015) Treatment of chronic hepatitis B with pattern recognition receptor agonists: current status and potential for a cure. Antivir Res 121:152–159

    PubMed  CAS  Google Scholar 

  • Charlesworth CT, Deshpande PS, Dever DP, Camarena J, Lemgart VT, Cromer MK, Vakulskas CA, Collingwood MA, Zhang L, Bode NM, Behlke MA, Dejene B, Cieniewicz B, Romano R, Lesch BJ, Gomez-Ospina N, Mantri S, Pavel-Dinu M, Weinberg KI, Porteus MH (2019) Identification of preexisting adaptive immunity to Cas9 proteins in humans. Nat Med 25:249–254

    PubMed  CAS  PubMed Central  Google Scholar 

  • Chaturvedi AK, Engels EA, Pfeiffer RM, Hernandez BY, Xiao W, Kim E et al (2011) Human papillomavirus and rising oropharyngeal cancer incidence in the United States. J Clin Oncol 29(32):4294

    PubMed  PubMed Central  Google Scholar 

  • Chen S, Lee B, Lee AY, Modzelewski AJ, He L (2016) Highly efficient mouse genome editing by CRISPR ribonucleoprotein electroporation of zygotes. J Biol Chem 291:14457–14467

    PubMed  PubMed Central  CAS  Google Scholar 

  • Chen JS, Dagdas YS, Kleinstiver BP, Welch MM, Sousa AA, Harrington LB, Sternberg SH, Joung JK, Yildiz A, Doudna JA (2017) Enhanced proofreading governs CRISPR–Cas9 targeting accuracy. Nature 550:407–410

    PubMed  PubMed Central  CAS  Google Scholar 

  • Chen YC, Sheng J, Trang P, Liu F (2018) Potential application of the CRISPR/Cas9 system against herpesvirus infections. Viruses 10:piiE291. https://doi.org/10.3390/v10060291

    Article  CAS  Google Scholar 

  • Cheng R, Peng J, Yan Y, Cao P, Wang J, Qiu C, Tang L, Liu D, Tang L, Jin J, Huang X, He F, Zhang P (2014) Highly efficient gene editing in adult mouse livers via adenoviral delivery of CRISPR/Cas9. FEBS Lett 588:3954–3958

    PubMed  CAS  Google Scholar 

  • Chomont N, El-Far M, Ancuta P, Trautmann L, Procopio FA, Yassine-Diab B, Schacker TW (2009) HIV reservoir size and persistence are driven by T cell survival and homeostatic proliferation. Nat Med 15(8):893

    PubMed  PubMed Central  CAS  Google Scholar 

  • Chou YY, Krupp A, Kaynor C, Gaudin R, Ma M, Cahir-McFarland E, Kirchhausen T (2016) Inhibition of JCPyV infection mediated by targeted viral genome editing using CRISPR/Cas9. Sci Rep 6:36921. https://doi.org/10.1038/srep36921

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chu VT, Weber T, Wefers B, Wurst W, Sander S, Rajewsky K, Kühn R (2015) Increasing the efficiency of homology-directed repair for CRISPR-Cas9-induced precise gene editing in mammalian cells. Nat Biotechnol 33:543–548

    PubMed  CAS  Google Scholar 

  • Cohen JI, Fauci AS, Varmus H, Nabel GJ (2011) Epstein Barr virus: an important vaccine target for cancer preventation. Sci Transl Med 3:107fs7. https://doi.org/10.1126/scitranslmed.3002878

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Colby DJ, Trautmann L, Pinyakorn S, Leyre L, Pagliuzza A, Kroon E et al (2018) Rapid HIV RNA rebound after antiretroviral treatment interruption in persons durably suppressed in Fiebig I acute HIV infection. Nat Med 24:923–926

    PubMed  PubMed Central  CAS  Google Scholar 

  • Craddock J, Heslop HE (2008) Adoptive cellular therapy with T cells specific for EBV-derived tumor antigens. Update Cancer Ther 3(1):33–41

    PubMed  PubMed Central  Google Scholar 

  • Crispo M, Mulet AP, Tesson L, Barrera N, Cuadro F, dos Santos-Neto PC, Nguyen TH, Crénéguy A, Brusselle L, Anegón I, Menchaca A (2015) Efficient generation of myostatin knock-out sheep using CRISPR/Cas9 technology and microinjection into zygotes. PLoS One 10:e0136690. https://doi.org/10.1371/journal.pone.0136690

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • D'Agostino Y, D'Aniello S (2017) Molecular basis, applications and challenges of CRISPR/Cas9: a continuously evolving tool for genome editing. Brief Funct Genomics 16:211–216

    PubMed  CAS  Google Scholar 

  • Damato EG, Winnen CW (2002) Cytomegalovirus infection: perinatal implications. J Obstet Gynecol Neonatal Nurs 31:86–92

    PubMed  Google Scholar 

  • Dandri M, Petersen J (2016) Mechanism of hepatitis B virus persistence in hepatocytes and its carcinogenic potential. Clin Infect Dis 62(suppl_4):S281–S288

    PubMed  PubMed Central  CAS  Google Scholar 

  • Darcis G, Das A, Berkhout B (2018) Tackling HIV persistence: pharmacological versus CRISPR-based shock strategies. Viruses 10(4):157

    PubMed Central  Google Scholar 

  • Dash PK, Kaminski R, Bella R, Hang S, Mathews S, Ahooyi TM, Chen C, Mancuso P, Sariyer R, Ferrante P, Donadoni M, Robinson JA, Sillman B, Lin Z, Hilaire JR, Banoub M, Elango M, Gautam N, Mosely RL, Poluektova LY, McMillan J, Bade AN, Gorantla S, Sariyer IK, Burdo TH, Young WB, Amini S, Gordon J, Jacobson JM, Edagwa B, Khalili K, Gendelman HE (2019) Sequential LASER ART and CRISPR treatments eliminate HIV-1 in a subset of infected humanized mice. Nat Commun. https://doi.org/10.2753//doi.org/10.1038/s41467-019-10366-y

  • Datta PK, Kaminiski R, Hu W, Pirrone V, Sullivan NT, Nonnemacher MR, Dampier W, Wigdahl B, Khalili K (2016) HIV-1 latency and eradication: past, present and future. Curr HIV Res 14:431–441

    PubMed  PubMed Central  CAS  Google Scholar 

  • Doll JR, Thompson RL, Sawtell NM (2019) Infectious herpes simplex virus in the brain stem is correlated with reactivation in the trigeminal ganglia. J Virol 93(8):e02209–e02218

    PubMed  PubMed Central  CAS  Google Scholar 

  • Dong C, Qu L, Wang H, Wei L, Dong Y, Xiong S (2015) Targeting hepatitis B virus cccDNA by CRISPR/Cas9 nuclease efficiently inhibits viral replication. Antivir Res 118:110–117

    PubMed  CAS  Google Scholar 

  • Drew WL (1988) Diagnosis of cytomegalovirus infection. Rev Infect Dis 10(Supplement_3):S468–S476

    PubMed  Google Scholar 

  • Dufour, C., Claudel, A., Joubarne, N., Merindol, N., Maisonnet, T., Masroori, N., ... Berthoux, L. (2018). Editing of the human TRIM5 gene to introduce mutations with the potential to inhibit HIV-1. PLoS One 13(1):e0191709

    PubMed  PubMed Central  Google Scholar 

  • Ebina H, Misawa N, Kanemura Y, Koyanagi Y (2013) Harnessing the CRISPR/Cas9 system to disrupt latent HIV-1 provirus. Sci Rep 3:2510. https://doi.org/10.1038/srep02510

    Article  PubMed  PubMed Central  Google Scholar 

  • Epstein MA (1964) Virus particles in cultured lymphoblasts from Burkitt's lymphoma. Lancet 1:702–703

    PubMed  CAS  Google Scholar 

  • Findlay GM, Boyle EA, Hause RJ, Klein JC, Shendure J (2014) Saturation editing of genomic regions by multiplex homology-directed repair. Nature 513:120–123

    PubMed  PubMed Central  CAS  Google Scholar 

  • Finzi D, Blankson J, Siliciano JD, Margolick JB, Chadwick K, Pierson T, ... Quinn TC (1999) Latent infection of CD4+ T cells provides a mechanism for lifelong persistence of HIV-1, even in patients on effective combination therapy. Nat Med 5(5): 512

    PubMed  CAS  Google Scholar 

  • Fisicaro P, Valdatta C, Massari M, Loggi E, Biasini E, Sacchelli L, ... Ferrari C (2010). Antiviral intrahepatic T-cell responses can be restored by blocking programmed death-1 pathway in chronic hepatitis B. Gastroenterology 138(2): 682–693

    Google Scholar 

  • Fu Y, Foden JA, Khayter C, Maeder ML, Reyon D, Joung JK, Sander JD (2013) High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol 31:822–826

    PubMed  PubMed Central  CAS  Google Scholar 

  • Gane EJ (2016) Future anti-HBV strategies. Liver Int 37:40–44

    Google Scholar 

  • Gaudelli NM, Komor AC, Rees HA, Packer MS, Badran AH, Bryson DI, Liu DR (2017) Programmable base editing of a•T to G•C in genomic DNA without DNA cleavage. Nature 551:464–471

    PubMed  PubMed Central  CAS  Google Scholar 

  • Gergen J, Coulon F, Creneguy A, Elain-Duret N, Gutierrez A, Pinkenburg O, Haspot F (2018) Multiplex CRISPR/Cas9 system impairs HCMV replication by excising an essential viral gene. PLoS One 13(2):e0192602

    PubMed  PubMed Central  Google Scholar 

  • Gilbert LA, Horlbeck MA, Adamson B, Villalta JE, Chen Y, Whitehead EH, Guimaraes C, Panning B, Ploegh HL, Bassik MC, Qi LS, Kampmann M, Weissman JS (2014) Genome-scale CRISPR-mediated control of gene repression and activation. Cell 159:647–661

    PubMed  PubMed Central  CAS  Google Scholar 

  • Gillison ML, Chaturvedi AK, Lowy DR (2008) HPV prophylactic vaccines and the potential prevention of noncervical cancers in both men and women. Cancer 113(S10):3036–3046

    PubMed  Google Scholar 

  • Gravitt PE (2012) Suppl 2: evidence and impact of human papillomavirus latency. Open Virol J 6:198

    PubMed  PubMed Central  Google Scholar 

  • Green JC, Hu JS (2017) Editing plants for virus resistance using CRISPR-Cas. Acta Virol 61:138–142

    PubMed  CAS  Google Scholar 

  • Griffin BD (2010) Marieke C. Verweij, and Emmanuel JHJ Wiertz. "herpesviruses and immunity: the art of evasion.". Vet Microbiol 143(1):89–100

    PubMed  CAS  Google Scholar 

  • Harden ME, Munger K (2017) Human papillomavirus molecular biology. Mutat Res 2017:3–12. https://doi.org/10.1016/j.mrrev.2016.07.002

    Article  CAS  Google Scholar 

  • Herrera-Carrillo E, Berkhout B (2016) Attacking HIV-1 RNA versus DNA by sequence-specific approaches: RNAi versus CRISPR-Cas. Biochem Soc Trans 44:1355–1365

    PubMed  CAS  Google Scholar 

  • Hilton IB, D'Ippolito AM, Vockley CM, Thakore PI, Crawford GE, Reddy TE, Gersbach CA (2015) Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers. Nat Biotechnol 33:510–517

    PubMed  PubMed Central  CAS  Google Scholar 

  • Hirano H, Gootenberg JS, Horii T, Abudayyeh OO, Kimura M, Hsu PD, Nakane T, Ishitani R, Hatada I, Zhang F, Nishimasu H, Nureki O (2016) Structure and engineering of Francisella novicida Cas9. Cell 164:950–961

    PubMed  PubMed Central  CAS  Google Scholar 

  • Ho YK, Zhi H, Bowlin T, Dorjbal B, Philip S, Zahoor MA, Shih HM, Semmes OJ, Schaefer B, Glover JN, Giam CZ (2015) HTLV-1 tax stimulates ubiquitin E3 ligase, ring finger protein 8, to assemble lysine 63-linked polyubiquitin chains for TAK1 and IKK activation. PLoS Pathog 11:e1005102. https://doi.org/10.1371/journal.ppat.1005102

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hong M, Murai Y, Kutsuna T, Takahashi H, Nomoto K, Cheng CM, Tsuneyama K (2006) Suppression of Epstein-Barr nuclear antigen 1 (EBNA1) by RNA interference inhibits proliferation of EBV-positive Burkitt’s lymphoma cells. J Cancer Res Clin Oncol 132(1):1–8

    PubMed  CAS  Google Scholar 

  • Horii T, Arai Y, Yamazaki M, Morita S, Kimura M, Itoh M, Abe Y, Hatada I (2014) Validation of microinjection methods for generating knockout mice by CRISPR/Cas-mediated genome engineering. Sci Rep 4:4513. https://doi.org/10.1038/srep04513

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hou P, Chen S, Wang S, Yu X, Chen Y, Jiang M, Zhuang K, Ho W, Hou W, Huang J, Guo D (2015) Genome editing of CXCR4 by CRISPR/cas9 confers cells resistant to HIV-1 infection. Sci Rep 5:15577. https://doi.org/10.1038/srep15577

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hsu PD, Scott DA, Weinstein JA, Ran FA, Konermann S, Agarwala V, Li Y, Fine EJ, Wu X, Shalem O, Cradick TJ, Marraffini LA, Bao G, Zhang F (2013) DNA targeting specificity of RNA-guided Cas9 nucleases. Nat Biotechnol 31:827–832

    PubMed  PubMed Central  CAS  Google Scholar 

  • Hsu PD, Lander ES, Zhang F (2014) Development and applications of CRISPR-Cas9 for genome engineering. Cell 157:1262–1278

    PubMed  PubMed Central  CAS  Google Scholar 

  • Hu W, Kaminski R, Yang F, Zhang Y, Cosentino L, Li F, Luo B, Alvarez-Carbonell D, Garcia-Mesa Y, Karn J, Mo X, Khalili K (2014a) RNA-directed gene editing specifically eradicates latent and prevents new HIV-1 infection. Proc Natl Acad Sci U S A 111:11461–11466

    PubMed  PubMed Central  CAS  Google Scholar 

  • Hu Z, Yu L, Zhu D, Ding W, Wang X, Zhang C, Wang L, Jiang X, Shen H, He D, Li K, Xi L, Ma D, Wang H (2014b) Disruption of HPV16 E7 by crispr/cas system induces apoptosis and growth inhibition in HPV 16 positive human cervical cancer cells. Biomed Res Int 2014:612823. https://doi.org/10.1155/2014/612823

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hung SS, Chrysostomou V, Li F, Lim JK, Wang JH, Powell JE, Tu L, Daniszewski M, Lo C, Wong RC, Crowston JG, Pébay A, King AE, Bui BV, Liu GS, Hewitt AW (2016) AAV-mediated CRISPR/Cas gene editing of retinal cells in vivo. Invest Ophthalmol Vis Sci 57:3470–3476

    PubMed  CAS  Google Scholar 

  • Ian MX, Lan SZ, Cheng ZF, Dan H, Qiong LH (2008) Suppression of EBNA1 expression inhibits growth of EBV positive NK/T cell lymphomas cells. Cancer Biol Ther 7(10):1602–1606

    PubMed  CAS  Google Scholar 

  • Ishino Y, Shinagawa H, Makino K, Amemura M, Nakata A (1987) Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. J Bacteriol 169(12):5429–5433

    PubMed  PubMed Central  CAS  Google Scholar 

  • Itzhaki RF (2018) Corroboration of a major role for herpes simplex virus type 1 in Alzheimer's disease. Front Aging Neurosci 10:324

    PubMed  PubMed Central  CAS  Google Scholar 

  • Jiang C, Mei M, Li B, Zhu X, Zu W, Tian Y, Wang Q, Guo Y, Dong Y, Tan X (2017) A non-viral CRISPR/Cas9 delivery system for therapeutically targeting HBV DNA and pcsk9 in vivo. Cell Res 27:440–443

    PubMed  PubMed Central  CAS  Google Scholar 

  • Kaminski R, Bella R, Yin C, Otte J, Ferrante P, Gendelman HE, Li H, Booze R, Gordon J, Hu W, Khalili K (2016a) Excision of HIV-1 DNA by gene editing: a proof-of-concept in vivo study. Gene Ther 23:696. https://doi.org/10.1038/gt.2016.45

    Article  PubMed  CAS  Google Scholar 

  • Kaminski R, Chen Y, Fischer T, Tedaldi E, Napoli A, Zhang Y, Karn J, Hu W, Khalili K (2016b) Elimination of HIV-1 genomes from human T-lymphoid cells by CRISPR/Cas9 gene editing. Sci Rep 6:22555. https://doi.org/10.1038/srep22555

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kanda T, Furuse Y, Oshitani H, Kiyono (2016) Highly efficient crispr/cas-mediated cloning and functional characterization of gastric cancer-derived epstein-barr virus strains. J Virol 90:4383–4393

    PubMed  PubMed Central  CAS  Google Scholar 

  • Kang H, Minder P, Park MA, Mesquitta WT, Torbett BE, Slukvin II (2015) CCR5 disruption in induced pluripotent stem cells using CRISPR/Cas9 provides selective resistance of immune cells to CCR5-tropic HIV-1 virus. Mol Ther Nucleic Acids 4:e268. https://doi.org/10.1038/mtna.2015.42

    Article  PubMed  CAS  Google Scholar 

  • Karimova M, Beschorner N, Dammermann W, Chemnitz J, Indenbirken D, Bockmann JH, Grundhoff A, Lüth S, Buchholz F, Schulze zur Wiesch J, Hauber J (2015) CRISPR/Cas9 nickase-mediated disruption of hepatitis B virus open reading frame S and X. Sci Rep 5:13734. https://doi.org/10.1038/srep13734

    Article  PubMed  PubMed Central  Google Scholar 

  • Kaushik A, Yndart A, Atluri V, Tiwari S, Tomitaka A, Gupta P, Jayant RD, Alvarez-Carbonell D, Khalili K, Nair M (2019) Magnetically guided non-invasive CRISPR-Cas9/gRNA delivery across blood-brain barrier to eradicate latent HIV-1 infection. Sci Rep 9:3928. https://doi.org/10.1038/s41598-019-40222-4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kennedy EM, Cullen BR (2015) Bacterial CRISPR/Cas DNA endonucleases: a revolutionary technology that could dramatically impact viral research and treatment. Virology 479-480:213–220

    PubMed  CAS  Google Scholar 

  • Kennedy EM, Cullen BR (2017) Gene editing: a new tool for viral disease. Annu Rev Med 68:401–411

    PubMed  CAS  Google Scholar 

  • Kennedy EM, Bassit LC, Mueller H, Kornepati AVR, Bogerd HP, Nie T, Chatterjee P, Javanbakht H, Schinazi RF, Cullen BR (2015) Suppression of hepatitis B virus DNA accumulation in chronically infected cells using a bacterial CRISPR/Cas RNA-guided DNA endonuclease. Virology 476:196–205

    PubMed  CAS  Google Scholar 

  • Kim D, Kim S, Kim S, Park J, Kim JS (2016) Genome-wide target specificities of CRISPR-Cas9 nucleases revealed by multiplex Digenome-seq. Genome Res 26:406–415

    PubMed  PubMed Central  CAS  Google Scholar 

  • Kleinstiver BP, Pattanayak V, Prew MS, Tsai SQ, Nguyen NT, Zheng Z, Joung JK (2016) High-fidelity CRISPR–Cas9 nucleases with no detectable genome-wide off-target effects. Nature 529:490–495

    PubMed  PubMed Central  CAS  Google Scholar 

  • Konermann S, Brigham MD, Trevino AE, Joung J, Abudayyeh OO, Barcena C, Hsu PD, Habib N, Gootenberg JS, Nishimasu H, Nureki O, Zhang F (2015) Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature 517:583–588

    PubMed  CAS  Google Scholar 

  • Lao YH, Li M, Gao MA, Shao D, Chi CW, Huang D, Chakraborty S, Ho TC, Jiang W, Wang HX, Wang S, Leong KW (2018) HPV oncogene manipulation using nonvirally delivered crispr/cas9 or Natronobacterium Gregoryi Argonaute. Adv Sci (Weinh) 5:1700540. https://doi.org/10.1002/advs.201700540

    Article  CAS  Google Scholar 

  • Le Rhun A, Escalera-Maurer A, Bratovič M, Charpentier E (2019) CRISPR-Cas in Streptococcus Pyogenes. RNA Biol 16:380–389

    PubMed  PubMed Central  Google Scholar 

  • Lebbink RJ, De Jong DC, Wolters F, Kruse EM, Van Ham PM, Wiertz EJ, Nijhuis M (2017) A combinational CRISPR/Cas9 gene-editing approach can halt HIV replication and prevent viral escape. Sci Rep 7:41968. https://doi.org/10.1038/srep41968

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lee C (2019) CRISPR/Cas9-based antiviral strategy: current status and the potential challenge. Molecules 24(7):1349

    PubMed Central  Google Scholar 

  • Lee MH, Chiou JF, Yen KY, Yang LL (2000) EBV DNA polymerase inhibition of tannins from Eugenia uniflora. Cancer Lett 154(2):131–136

    PubMed  CAS  Google Scholar 

  • Lee S, Loecher M, Iyer R (2018) Immunomodulation in hepatocellular cancer. J Gastrointest Oncol 9(1):208

    PubMed  PubMed Central  Google Scholar 

  • Li C, Guan X, Du T, Jin W, Wu B, Liu Y, Wang P, Hu B, Griffin GE, Shattock RJ, Hu Q (2015) Inhibition of HIV-1 infection of primary CD4+ T-cells by gene editing of CCR5 using adenovirus-delivered CRISPR/Cas9. J Gen Virol 96:2381–2393

    PubMed  CAS  Google Scholar 

  • Li H, Sheng C, Wang S, Yang L, Liang Y, Huang Y, Liu H, Li P, Yang C, Yang X, Jia L, Xie J, Wang L, Hao R, Du X, Xu D, Zhou J, Li M, Sun Y, Tong Y, Li Q, Qiu S, Song H (2017) Removal of integrated hepatitis B virus DNA using CRISPR-Cas9. Front Cell Infect Microbiol 7:91. https://doi.org/10.3389/fcimb.2017.00091

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liao HK, Gu Y, Diaz A, Marlett J, Takahashi Y, Li M, Suzuki K, Xu R, Hishida T, Chang CJ, Esteban CR, Young J, Izpisua Belmonte JC (2015) Use of the CRISPR/Cas9 system as an intracellular defense against HIV-1 infection in human cells. Nat Commun 6:6413. https://doi.org/10.1038/ncomms7413

    Article  PubMed  CAS  Google Scholar 

  • Lin SR, Yang HC, Kuo YT, Liu CJ, Yang TY, Sung KC, Lin YY, Wang HY, Wang CC, Shen YC, Wu FY, Kao JH, Chen DS, Chen PJ (2014) The CRISPR/Cas9 system facilitates clearance of the intrahepatic HBV templates in vivo. Mol Ther Nucleic Acids 3:e186. https://doi.org/10.1038/mtna.2014.38

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lin C, Li H, Hao M, Xiong D, Luo Y, Huang C, Yuan Q, Zhang J, Xia N (2016) Increasing the efficiency of crispr/cas9 –mediated precise genome editing of HSV-1 virus in human cels. Sci Rep 6:34531. https://doi.org/10.1038/srep34531

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lino CA, Harper JC, Carney JP, Timlin JA (2018) Delivering CRISPR: a review of the challenges and approaches. Drug Deliv 25:1234–1257

    PubMed  PubMed Central  CAS  Google Scholar 

  • Liu C, Zhang L, Liu H, Cheng K (2017) Delivery strategies of the CRISPR-Cas9 gene-editing system for therapeutic applications. J Control Release 266:17–26

    PubMed  PubMed Central  CAS  Google Scholar 

  • Liu Y, Zhao M, Gong M, Xu Y, Xie C, Deng H, Li X, Wu H, Wang Z (2018) Inhibition of hepatitis B virus replication via HBV DNA cleavage by Cas9 from Staphylococcus aureus. Antivir Res 152:58–67

    PubMed  CAS  Google Scholar 

  • Long C, Amoasii L, Mireault AA, McAnally JR, Li H, Sanchez-Ortiz E, Bhattacharyya S, Shelton JM, Bassel-Duby R, Olson EN (2016) Postnatal genome editing partially restores dystrophin expression in a mouse model of muscular dystrophy. Science 351:400–403

    PubMed  CAS  Google Scholar 

  • Lopatin U (2019) Drugs in the pipeline for HBV. Clin Liver Dis 23(2019):535–555

    PubMed  Google Scholar 

  • Maartens G, Celum C, Lewin SR (2014) HIV infection: epidemiology, pathogenesis, treatment, and prevention. Lancet 384(9939):258–271

    PubMed  Google Scholar 

  • Maddalo D, Manchado E, Concepcion CP, Bonetti C, Vidigal JA, Han YC, Ogrodowski P, Crippa A, Rekhtman N, De Stanchina E, Lowe SW, Ventura A (2014) In vivo engineering of oncogenic chromosomal rearrangements with the CRISPR/Cas9 system. Nature 516:423–427

    PubMed  PubMed Central  CAS  Google Scholar 

  • Maggio I, Stefanucci L, Janssen JM, Liu J, Chen X, Mouly V, Gonçalves MA (2016) Selection-free gene repair after adenoviral vector transduction of designer nucleases: rescue of dystrophin synthesis in DMD muscle cell populations. Nucleic Acids Res 44:1449–1470

    PubMed  PubMed Central  CAS  Google Scholar 

  • Maglennon GA, McIntosh P, Doorbar J (2011) Persistence of viral DNA in the epithelial basal layer suggests a model for papillomavirus latency following immune regression. Virology 414(2):153–163

    PubMed  CAS  Google Scholar 

  • Mali P, Aach J, Stranges PB, Esvelt KM, Moosburner M, Kosuri S, Yang L, Church GM (2013) CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat Biotechnol 31:833–838

    PubMed  PubMed Central  CAS  Google Scholar 

  • Manglani M, McGavern DB (2018) New advances in CNS immunity against viral infection. Curr Opin Virol 28:116–126

    PubMed  CAS  Google Scholar 

  • Maruyama T, Dougan SK, Truttmann MC, Bilate AM, Ingram JR, Ploegh HL (2015) Increasing the efficiency of precise genome editing with CRISPR-Cas9 by inhibition of nonhomologous end joining. Nat Biotechnol 34:210. https://doi.org/10.1038/nbt0216-210c

    Article  CAS  Google Scholar 

  • Matano M, Date S, Shimokawa M, Takano A, Fujii M, Ohta Y, Watanabe T, Kanai T, Sato T (2015) Modeling colorectal cancer using CRISPR-Cas9–mediated engineering of human intestinal organoids. Nat Med 21:256–262

    PubMed  CAS  Google Scholar 

  • Mefferd AL, Bogerd HP, Irwan ID, Cullen BR (2018) Insights into the mechanisms underlying the inactivation of HIV-1 proviruses by CRISPR/Cas. Virology 520:116–126

    PubMed  CAS  Google Scholar 

  • Mojica FJ (2000) Biological significance of a family of regularly spaced repeats in the genomes of archaea, Bacteria and mitochondria. Mol Microbiol 36(1):244–246

    PubMed  CAS  Google Scholar 

  • Mojica FJ, Díez-Villaseñor C, García-Martínez J, Soria E (2005) Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J Mol Evol 60:174–182

    PubMed  CAS  Google Scholar 

  • Nath A, Tyler KL (2013) Novel approaches and challenges to treatment of central nervous system viral infections. Ann Neurol 74:412–422

    PubMed  PubMed Central  CAS  Google Scholar 

  • Nelson CE, Hakim CH, Ousterout DG, Thakore PI, Moreb EA, Castellanos Rivera RM, Madhavan S, Pan X, Ran FA, Yan WX, Asokan A, Zhang F, Duan D, Gersbach CA (2016) In vivo genome editing improves muscle function in a mouse model of Duchenne muscular dystrophy. Science 351:403–407

    PubMed  CAS  Google Scholar 

  • Nicoll MP, Proença JT, Efstathiou S (2012) The molecular basis of herpes simplex virus latency. FEMS Microbiol Rev 36(3):684–705

    PubMed  CAS  Google Scholar 

  • O'Connell MR, Oakes BL, Sternberg SH, East-Seletsky A, Kaplan M, Doudna JA (2014) Programmable RNA recognition and cleavage by CRISPR/Cas9. Nature 516:263–266

    PubMed  PubMed Central  CAS  Google Scholar 

  • Panfil AR, London JA, Green PL, Yoder KE (2018) CRISPR/Cas9 genome editing to disable the latent HIV-1 provirus. Front Microbiol 9:3107. https://doi.org/10.3389/fmicb.2018.03107

    Article  PubMed  PubMed Central  Google Scholar 

  • Pebody RG, Andrews N, Brown D, Gopal R, De Melker H, François G, ... Kojouharova M (2004). The seroepidemiology of herpes simplex virus type 1 and 2 in Europe. Sex Transm Infect 80(3): 185–191

    PubMed  PubMed Central  CAS  Google Scholar 

  • Platt RJ, Chen S, Zhou Y, Yim MJ, Swiech L, Kempton HR, Dahlman JE, Parnas O, Eisenhaure TM, Jovanovic M, Graham DB, Jhunjhunwala S, Heidenreich M, Xavier RJ, Langer R, Anderson DG, Hacohen N, Regev A, Feng G, Sharp PA, Zhang F (2014) CRISPR-Cas9 knockin mice for genome editing and cancer modeling. Cell 159:440–455

    PubMed  PubMed Central  CAS  Google Scholar 

  • Pourcel C, Salvignol G, Vergnaud G (2005) CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology 151:653–663

    PubMed  CAS  Google Scholar 

  • Price AA, Sampson TR, Ratner HK, Grakoui A, Weiss DS (2015) Cas9-mediated targeting of viral RNA in eukaryotic cells. Proc Natl Acad Sci U S A 112:6164–6169

    PubMed  PubMed Central  CAS  Google Scholar 

  • Qin W, Dion SL, Kutny PM, Zhang Y, Cheng AW, Jillette NL, Malhotra A, Geurts AM, Chen YG, Wang H (2015) Efficient CRISPR/Cas9-mediated genome editing in mice by zygote electroporation of nuclease. Genetics 200:423–430

    PubMed  PubMed Central  CAS  Google Scholar 

  • Raab-Traub N (2012) Novel mechanisms of EBV-induced oncogenesis. Curr Opin Virol 2:453–458

    PubMed  PubMed Central  CAS  Google Scholar 

  • Raveux A, Vandormael-Pournin S, Cohen-Tannoudji M (2017) Optimization of the production of knock-in alleles by CRISPR/Cas9 microinjection into the mouse zygote. Sci Rep 7:42661. https://doi.org/10.1038/srep42661

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Reeves MB, Lehner PJ, Sissons JGP, Sinclair JH (2005) An in vitro model for the regulation of human cytomegalovirus latency and reactivation in dendritic cells by chromatin remodelling. J Gen Virol 86(11):2949–2954

    PubMed  CAS  Google Scholar 

  • Revello MG, Zavattoni M, Furione M, Fabbri E, Gerna G (2006) Preconceptional primary human cytomegalovirus infection and risk of congenital infection. J Infect Dis 193:783–787

    PubMed  Google Scholar 

  • Roehm PC, Shekarabi M, Wollebo HS, Bellizzi A, He L, Salkind J, Khalili K (2016) Inhibition of HSV-1 replication by gene editing strategy. Sci Rep 6:23146. https://doi.org/10.1038/srep23146

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Romero JR, Newland JG (2003) Viral meningitis and encephalitis: traditional and emerging viral agents. Semin Pediatr Infect Dis 14:72–82

    PubMed  Google Scholar 

  • Rubin RH (1990) Impact of cytomegalovirus infection on organ transplant recipients. Rev Infect Dis 12(Supplement_7):S754–S766

    PubMed  Google Scholar 

  • Russell TA, Stefanovic T, Tscharke DC (2015) Engineering herpes simplex viruses by infection–transfection methods including recombination site targeting by CRISPR/Cas9 nucleases. J Virol Methods 213:18–25

    PubMed  CAS  Google Scholar 

  • Sakuma T, Nishikawa A, Kume S, Chayama K, Yamamoto T (2014) Multiplex genome engineering in human cells using all-in-one CRISPR/Cas9 vector system. Sci Rep 4:5400. https://doi.org/10.1038/srep05400

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sakuma T, Masaki K, Abe-Chayama H, Mochida K, Yamamoto T, Chayama K (2016) Highly multiplexed CRISPR-Cas9-nuclease and Cas9-nickase vectors for inactivation of hepatitis B virus. Genes Cells 21:1253–1262

    PubMed  CAS  Google Scholar 

  • Sanders VJ, Waddell AE, Felisan SL, Li X, Conrad AJ, Tourtellotte WW (1996) Herpes simplex virus in postmortem multiple sclerosis brain tissue. Arch Neurol 53(2):125–133

    PubMed  CAS  Google Scholar 

  • Sanders VJ, Felisan SL, Waddell AE, Conrad AJ, Schmid P, Swartz BE ... Tourtellotte WW (1997) Presence of herpes simplex DNA in surgical tissue from human epileptic seizure foci detected by polymerase chain reaction: preliminary study. Arch Neurol 54(8) 954–960

    PubMed  CAS  Google Scholar 

  • Satou Y, Miyazato P, Ishihara K, Yaguchi H, Melamed A, Miura M, Fukuda A, Nosaka K, Watanabe T, Rowan AG, Nakao M, Bangham CR (2016) The retrovirus HTLV-1 inserts an ectopic CTCF-binding site into the human genome. Proc Natl Acad Sci U S A 113:3054–3059

    PubMed  PubMed Central  CAS  Google Scholar 

  • Savic N, Ringnalda FC, Lindsay H, Berk C, Bargsten K, Li Y ... Jinek M (2018) Covalent linkage of the DNA repair template to the CRISPR-Cas9 nuclease enhances homology-directed repair. Elife 7: e33761

  • Sawtell NM (1997) Comprehensive quantification of herpes simplex virus latency at the single-cell level. J Virol 71(7):5423–5431

    PubMed  PubMed Central  CAS  Google Scholar 

  • Seeger C, Sohn JA (2014) Targeting hepatitis B virus with CRISPR/Cas9. Mol Ther-Nucleic Acids 3:e216

    PubMed  PubMed Central  CAS  Google Scholar 

  • Shalem O, Sanjana NE, Hartenian E, Shi X, Scott DA, Mikkelson T, Heckl D, Ebert BL, Root DE, Doench JG, Zhang F (2014) Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 343:84–87

    CAS  PubMed  Google Scholar 

  • Shan L, Deng K, Shroff NS, Durand CM, Rabi SA, Yang HC ... Siliciano RF (2012) Stimulation of HIV-1-specific cytolytic T lymphocytes facilitates elimination of latent viral reservoir after virus reactivation. Immunity 36(3): 491–501

    PubMed  PubMed Central  CAS  Google Scholar 

  • Singh P, Schimenti JC, Bolcun-Filas E (2015) A mouse geneticist’s practical guide to CRISPR applications. Genetics 199:1–15

    PubMed  CAS  Google Scholar 

  • Sinzger C, Digel M, Jahn G (2008) Cytomegalovirus cell tropism. Curr Top Microbiol Immunol 325:63–83. https://doi.org/10.1007/978-3-540-77349.8_4

    Article  PubMed  CAS  Google Scholar 

  • Slaymaker IM, Gao L, Zetsche B, Scott DA, Yan WX, Zhang F (2016) Rationally engineered Cas9 nucleases with improved specificity. Science 351:84–88

    PubMed  CAS  Google Scholar 

  • Song J, Zhang X, Ge Q, Yuan C, Chu L, Liang HF, Liao Z, Liu Q, Zhang Z, Zhang B (2018) CRISPR/Cas9- mediated knockout of HBsAg inhibit proliferation and and tumorigenicity of HBV-positive hepatocellular carcinoma cells. J Cell Biochem 119:8419–8431

    PubMed  PubMed Central  CAS  Google Scholar 

  • Soppe JA, Lebbink RJ (2017) Antiviral goes viral: harnessing CRISPR/Cas9 to combat viruses in humans. Trends Microbiol 25:833–850

    PubMed  CAS  Google Scholar 

  • Srivastava M, Nambiar M, Sharma S, Karki SS, Goldsmith G, Hegde M, Kumar S, Pandey M, Singh RK, Ray P, Natarajan R, Kelkar M, De A, Choudhary B, Raghavan SC (2012) An inhibitor of nonhomologous end-joining abrogates double-strand break repair and impedes cancer progression. Cell 151:1474–1487

    PubMed  CAS  Google Scholar 

  • Stern L, Withers B, Avdic S, Gottlieb D, Abendroth A, Blyth E, Slobedman B (2019) Human Cytomegalovirus latency and reactivation in allogeneic hematopoietic stem cell transplant recipients. Front Microbiol. https://doi.org/10.3389/fmicb.2019.01186

  • Strecker J, Ladha A, Gardner Z, Schmid-Burgk JL, Makarova KS, Koonin EV, Zhang F (2019) RNA-guided DNA insertion with CRISPR-associated transposases. Science. https://doi.org/10.1126/science.aax9181

    PubMed  PubMed Central  CAS  Google Scholar 

  • Strutt SC, Torrez RM, Kaya E, Negrete OA, Doudna JA (2018) RNA-dependent RNA targeting by CRISPR-Cas9. Elife 7pii:e32724. https://doi.org/10.7554/eLife.32724

    Article  Google Scholar 

  • Swiech L, Heidenreich M, Banerjee A, Habib N, Li Y, Trombetta J, Sur M, Zhang F (2015) In vivo interrogation of gene function in the mammalian brain using CRISPR-Cas9. Nat Biotechnol 33:102–106

    PubMed  CAS  Google Scholar 

  • Tabebordbar M, Zhu K, Cheng JKW, Chew WL, Widrick JJ, Yan WX, Maesner C, Wu EY, Xiao R, Ran FA, Cong L, Zhang F, Vandenberghe LH, Church GM, Wagers AJ (2016) In vivo gene editing in dystrophic mouse muscle and muscle stem cells. Science 351:407–411

    PubMed  CAS  Google Scholar 

  • Tang L, Zhao Q, Wu S, Cheng J, Chang J, Guo JT (2017) The current status and future directions of hepatitis B antiviral drug discovery. Expert Opin Drug Discovery 12(1):5–15

    CAS  Google Scholar 

  • Tavazzi E, White MK, Khalili K (2012) Progressive multifocal leukoencephalopathy: clinical and molecular aspects. Rev Med Virol 22:18–32

    PubMed  Google Scholar 

  • Thompson RL, Sawtell NM (2010) Therapeutic implications of new insights into the critical role of VP16 in initiating the earliest stages of HSV reactivation from latency. Future Med Chem 2(7):1099–1105

    PubMed  CAS  Google Scholar 

  • Thompson S, Messick T, Schultz DC, Reichman M, Lieberman PM (2010) Development of a high-throughput screen for inhibitors of Epstein-Barr virus EBNA1. J Biomol Screen 15(9):1107–1115

    PubMed  PubMed Central  CAS  Google Scholar 

  • Tsai SQ, Zheng Z, Nguyen NT, Liebers M, Topkar VV, Thapar V, Wyvekens N, Khayter C, Iafrate AJ, Le LP, Aryee MJ, Joung JK (2015) GUIDE-seq enables genome-wide profiling of off-target cleavage by CRISPR-Cas nucleases. Nat Biotechnol 33:187–197

    PubMed  CAS  Google Scholar 

  • Ueda S, Ebina H, Kanemura Y, Misawa N, Koyanagi Y (2016) Anti-HIV-1 potency of the CRISPR/Cas9 system insufficient to fully inhibit viral replication. Microbiol Immunol 60:483–496

    PubMed  CAS  Google Scholar 

  • van Diemen FR, Kruse EM, Hooykaas MJ, Bruggeling CE, Schürch AC, van Ham PM, Imhof SM, Nijhuis M, Wiertz EJ, Lebbink RJ (2016) Crispr/cas9-mediated genome editing of herpesviruses limits productive and latent infections. PLoS Pathog 12:e1005701. https://doi.org/10.1371/journal.ppat.1005701

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Voets O, Tielen F, Elstak E, Benschop J, Grimbergen M, Stallen J, Janssen R, van Marle A, Essrich C (2017) Highly efficient gene inactivation by adenoviral CRISPR/Cas9 in human primary cells. PLoS One 12:e0182974. https://doi.org/10.1371/journal.pone.0182974

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vora S, Tuttle M, Cheng J, Church G (2016) Next stop for the CRISPR revolution: RNA-guided epigenetic regulators. FEBS J 283:3181–3193

    PubMed  CAS  Google Scholar 

  • Wald A, Corey L (2007) Persistence in the population: epidemiology, transmission. In: Arvin A, Campadelli-Fiume G, Mocarski E, Moore PS, Roizman B, Whitley R, Yamanishi K (eds) Human herpesviruses: biology, therapy, and Immunoprophylaxis. Cambridge University Press, Cambridge Chapter 36

    Google Scholar 

  • Wang J, Quake SR (2014) Rna-guided endonuclease provides a therapeutic strategy to cure latent herpesviridae infection. Proc Natl Acad Sci U S A 111:13157–13162

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wang H, Yang H, Shivalila CS, Dawlaty MM, Cheng AW, Zhang F, Jaenisch R (2013) One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153:910–918

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wang W, Ye C, Liu J, Zhang D, Kimata JT, Zhou P (2014) CCR5 gene disruption via lentiviral vectors expressing Cas9 and single guided RNA renders cells resistant to HIV-1 infection. PLoS One 9:e115987. https://doi.org/10.1371/journal.pone.0115987

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang G, Zhao N, Berkhout B, Das AT (2016a) A combinatorial CRISPR Cas9 attack on HIV-1 DNA extinguishes all infectious provirus in infected T cell cultures. Cell Rep 17:2819–2826

    PubMed  CAS  Google Scholar 

  • Wang G, Zhao N, Berkhout B, Das AT (2016b) CRISPR-Cas9 can inhibit HIV-1 replication but NHEJ repair facilitates virus escape. Mol Ther 24:522–526

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wang M, Zuris JA, Meng F, Rees H, Sun S, Deng P, Han Y, Gao X, Pouli D, Wu Q, Georgakoudi I, Liu DR, Xu Q (2016c) Efficient delivery of genome editing proteins using bioreducible lipid nanoparticles. Proc Natl Acad Sci U S A 113:2868–2873

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wang G, Zhao N, Berkhout B, Das AT (2018a) CRISPR-Cas based antiviral strategies against HIV-1. Virus Res 244:321–332

    PubMed  CAS  Google Scholar 

  • Wang Y, Liu KI, Sutrisnoh NB, Srinivasan H, Zhang J, Li J, Zhang F, Lalith CRJ, Xing H, Shanmugam R, Foo JN, Yeo HT, Ooi KH, Bleckwehl T, Par YYR, Lee SM, Ismail NNB, Sanwari NAB, Lee STV, Lew J, Tan MH (2018b) Systematic evaluation of CRISPR-Cas systems reveals design principles for genome editing in human cells. Genome Biol 19:62. https://doi.org/10.1186/s13059-018-1445-x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wen Y, Bar KJ, Li JZ (2018) Lessons learned from HIV antiretroviral treatment interruption trials. Curr Opin HIV AIDS 13:416–421

    PubMed  Google Scholar 

  • White MK, Khalili K (2011) Pathogenesis of progressive multifocal leukoencephalopathy—revisited. J Infect Dis 203(5):578–586

    PubMed  PubMed Central  Google Scholar 

  • White MK, Gordon J, Khalili K (2013) The rapidly expanding family of human polyomaviruses: recent developments in understanding their life cycle and role in human pathology. PLoS Pathog 9(3):e1003206

    PubMed  PubMed Central  CAS  Google Scholar 

  • White MK, Kaminski R, Wollebo H, Hu W, Malcolm T, Khalili K (2016) Gene editing for treatment of neurological infections. Neurotherapeutics 13:547–554

    PubMed  PubMed Central  CAS  Google Scholar 

  • Whitehurst CB, Sanders MK, Law M, Wang FZ, Xiong J, Dittmer DP, Pagano JS (2013) Maribavir inhibits Epstein-Barr virus transcription through the EBV protein kinase. J Virol 87(9):5311–5315

    PubMed  PubMed Central  CAS  Google Scholar 

  • Whitley RJ, Roizman B (2001) Herpes simplex virus infections. Lancet 357:1513–1518

    PubMed  CAS  Google Scholar 

  • Wiedenheft B, Sternberg SH, Doudna JA (2012) RNA-guided genetic silencing systems in bacteria and archaea. Nature 482(7385):331

    PubMed  CAS  Google Scholar 

  • Wightman F, Solomon A, Khoury G, Green JA, Gray L, Gorry PR ... Cameron PU (2010). Both CD31+ and CD31-naive CD4+ T cells are persistent HIV type 1-infected reservoirs in individuals receiving antiretroviral therapy. J Infect Dis 202(11): 1738–1748

    PubMed  Google Scholar 

  • Wollebo HS, Bellizzi A, Kaminiski R, Hu W, White MK, Khalili K (2015a) Crisper/Cas9 system as an agent for eliminating polyomavirus JC infection. PLoS One 10(9):e0136046. https://doi.org/10.1371/journal.pone.0136046

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wollebo HS, White MK, Gordon J, Berger JR, Khalili K (2015b) Persistence and pathogenesis of the neurotropic polyomavirus JC. Ann Neurol 77:560–570

    PubMed  PubMed Central  Google Scholar 

  • Wu X, Kriz AJ, Sharp PA (2014) Target specificity of the CRISPR-Cas9 system. Quant Biol 2:59–70

    PubMed  PubMed Central  CAS  Google Scholar 

  • Xu F, Schillinger JA, Sternberg MR, Johnson RE, Lee FK, Nahmias AJ, Markowitz LE (2002) Seroprevalence and coinfection with herpes simplex virus type 1 and type 2 in the United States, 1988–1994. J Infect Dis 185(8):1019–1024

    PubMed  Google Scholar 

  • Xu X, Fan S, Zhou J, Zhang Y, Che Y, Cai H, Wang L, Guo L, Liu L, Li Q (2016) The mutated tegument protein U17 attenuates the virulence of herpes simplex virus 1 by reducing the modulation of alpha-4 gene transcription. Virol J 13:152. https://doi.org/10.1186/s12985-016-0600-9

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yamano T, Nishimasu H, Zetsche B, Hirano H, Slaymaker IM, Li Y, Fedorova I, Nakane T, Makarova KS, Koonin EV, Ishitani R, Zhang F, Nureki O (2016) Crystal structure of Cpf1 in complex with guide RNA and target DNA. Cell 165:949–962

    PubMed  PubMed Central  CAS  Google Scholar 

  • Yan WX, Hunnewell P, Alfonse LE, Carte JM, Keston-Smith E, Sothiselvam S, Garrity AJ, Chong S, Makarova KS, Koonin EV, Cheng DR, Scott DA (2019) Functionally diverse type V CRISPR-Cas systems. Science 363:88–91

    PubMed  CAS  Google Scholar 

  • Yang HC, Chen PJ (2018) The potential and challenges of CRISPR-Cas9 in eradication of hepatisis B virus covalently closed circular DNA. Virus Res 244:304–310

    PubMed  CAS  Google Scholar 

  • Yao S, He Z, Chen C (2015) CRISPR/Cas9-mediated genome editing of epigenetic factors for cancer therapy. Hum Gene Ther 26:463–471

    PubMed  CAS  Google Scholar 

  • Yin H, Song CQ, Dorkin JR, Zhu LJ, Li Y, Wu Q, Park A, Yang J, Suresh S, Bizhanova A, Gupta A, Bolukbasi MF, Walsh S, Bogorad RL, Gao G, Weng Z, Dong Y, Koteliansky V, Wolfe SA, Langer R, Xue W, Anderson DG (2016) Therapeutic genome editing by combined viral and non-viral delivery of CRISPR system components in vivo. Nat Biotechnol 34:328–333

    PubMed  PubMed Central  CAS  Google Scholar 

  • Yin C, Zhang T, Qu X, Zhang Y, Putatunda R, Xiao X et al (2017) In vivo excision of HIV-1 provirus by saCas9 and multiplex single-guide RNAs in animal models. Mol Ther 25(5):1168–1186

    PubMed  PubMed Central  CAS  Google Scholar 

  • Yoder KE, Bundschuh R (2016) Host double strand break repair generates HIV-1 strains resistant to CRISPR/Cas9. Sci Rep 6:29530. https://doi.org/10.1038/srep29530

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yoshiba T, Saga Y, Urabe M, Uchibori R, Matsubara S, Fujiwara H, Mizukami H (2019) CRISPR/Cas9-mediated cervical cancer treatment targeting human papillomavirus E6. Oncol Lett 17:2197–2206

    PubMed  CAS  Google Scholar 

  • Yuen KS, Chan CP, Kok KH, Jin DY (2017) Mutagenesis and genome engineering of Epstein–Barr virus in cultured human cells by CRISPR/Cas9. Methods Mol Biol 1498:23–31

    PubMed  CAS  Google Scholar 

  • Yuen KS, Wang ZM, Wong NHM, Zhang ZQ, Cheng TF, Lui WY et al (2018a) Suppression of Epstein-Barr virus DNA load in latently infected nasopharyngeal carcinoma cells by CRISPR/Cas9. Virus Res 244:296–303

    PubMed  CAS  Google Scholar 

  • Yuen KS, Wang ZM, Wong NM, Zhang ZQ, Cheng TF, Lui WY, Chan CP, Jin DY (2018b) Suppression of Epstein-Barr virus DNA load in latently infected nasopharyngeal carcinoma cells by CRISPR/Cas9. Virus Res 244:296–303

    PubMed  CAS  Google Scholar 

  • Zaidi SS, Tashkandi M, Mansoor S, Mahfouz MM (2016) Engineering plant immunity: using CRISPR/Cas9 to generate virus resistance. Front Plant Sci 7:1673. https://doi.org/10.3389/fpls.2016.01673

    Article  PubMed  PubMed Central  Google Scholar 

  • Zetsche B, Gootenberg JS, Abudayyeh OO, Slaymaker IM, Makarova KS, Essletzbichler P, Volz SE, Joung J, van der Oost J, Regev A, Koonin EV, Zhang F (2015) Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163:759–771

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang Y, Yin C, Zhang T, Li F, Yang W, Kaminski R, Hu W (2015) CRISPR/gRNA-directed synergistic activation mediator (SAM) induces specific, persistent and robust reactivation of the HIV-1 latent reservoirs. Sci Rep 5:16277

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang D, Li Z, Li JF (2016) Targeted gene manipulation in plants using the CRISPR/Cas technology. J Genet Genomics 43:251–262

    PubMed  Google Scholar 

  • Zhen S, Li X (2017) Oncogenic human papillomavirus: application of CRISPR/Cas9 therapeutic strategies for cervical cancer. Cell Physiol Biochem 44:2455–2466

    PubMed  CAS  Google Scholar 

  • Zhen S, Hua L, Liu YH, Gao LC, Fu J, Wan DY, Dong LH, Song HF, Gao X (2015) Harnessing the clustered regularly interspaced short palindromic repeat (CRISPR)/CRISPR-associated Cas9 system to disrupt the hepatitis B virus. Gene Ther 22:404–412

    PubMed  CAS  Google Scholar 

  • Zhen S, Lu JJ, Wang LJ, Sun XM, Zhang JQ, Li X, Luo WJ, Zhao L (2016) In vitro and in vivo synergistic therapeutic effect of cisplatin with human papillomavirus 16 E6/E7 CRISPR/Cas9 on cervical Cancer cell line. Transl Oncol 9:498–504

    PubMed  PubMed Central  Google Scholar 

  • Zhu W, Lei R, Le Duff Y, Li J, Guo F, Wainberg MA, Liang C (2015) The CRISPR/Cas9 system inactivates latent HIV-1 proviral DNA. Retrovirology 12:22. https://doi.org/10.1186/s12977-015-0150-z

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhu D, Pan C, Sheng J, Liang H, Bian Z, Liu Y (2018) Human cytomegalovirus reprograms haematopoietic progenitor cells into immunosuppressive monocytes to achieve latency. Nat Microbiol 3:503–513. https://doi.org/10.1038/s41564-018-0131-9

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zuckermann M, Hovestadt V, Knobbe-Thomsen CB, Zapatka M, Northcott PA, Schramm K, Belic J, Jones DT, Tschida B, Moriarity B, Largaespada D, Roussel MF, Korshunov A, Reifenberger G, Pfister SM, Lichter P, Kawauchi D, Gronych J (2015) Somatic CRISPR/Cas9-mediated tumour suppressor disruption enables versatile brain tumour modelling. Nat Commun 6:7391. https://doi.org/10.1038/ncomms8391

    Article  PubMed  CAS  Google Scholar 

  • Zuris JA, Thompson DB, Shu Y, Guilinger JP, Bessen JL, Hu JH, Maeder ML, Joung JK, Chen ZY, Liu DR (2015) Cationic lipid-mediated delivery of proteins enables efficient protein-based genome editing in vitro and in vivo. Nat Biotechnol 33:73–80

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank past and present members of the Center for Neurovirology for their insightful discussion and sharing of ideas. This work was supported by seed money from Temple University awarded to HSW.

Author information

Authors and Affiliations

  1. Center for Neurovirology, Department of Neuroscience, Lewis Katz School of Medicine at Temple University, Room 756 MERB, 3500 N. Broad Street, Philadelphia, PA, 19140, USA

    Anna Bellizzi, Nicholas Ahye, Gauthami Jalagadugula & Hassen S. Wollebo

Authors
  1. Anna Bellizzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nicholas Ahye
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gauthami Jalagadugula
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hassen S. Wollebo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hassen S. Wollebo.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bellizzi, A., Ahye, N., Jalagadugula, G. et al. A Broad Application of CRISPR Cas9 in Infectious Diseases of Central Nervous System. J Neuroimmune Pharmacol 14, 578–594 (2019). https://doi.org/10.1007/s11481-019-09878-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11481-019-09878-7

Keywords

Search

Navigation